Distinguishing features

Furoviruses have a bipartite genome, a “30K”-like cell-to-cell movement protein and are transmitted by root-infecting vectors in the family Plasmodiphorales, once described as fungi but now classified as Cercozoa.

Virion

Morphology

Virions are non-enveloped hollow rods, which have helical symmetry. Virions are about 20 nm in diameter, with predominant lengths of 140–160 nm and 260–300 nm. The length distribution of the soil-borne wheat mosaic virus (SBWMV) short particles is broad, 80–160 nm, due to the presence of deletion mutants in some cultures (Figure 1.Furovirus).

Nucleic acid

Complete or almost complete sequences are available for isolates representing all species in the genus [{Shirako and Wilson 1993:8317092RJOHTXShirako and Wilson 1993, Complete nucleotide sequence and organization of the bipartite RNA genome of soil-borne wheat mosaic virus, Virology, 195, 1, 16-32RJOMREFDiao et al., 1999:10497118RJOHTXDiao et al., 1999, Sequences of European wheat mosaic virus and oat golden stripe virus and genome analysis of the genus Furovirus, Virology, 261, 2, 331-9RJOMREFShirako et al., 2000:10772992RJOHTXShirako et al., 2000, Similarity and divergence among viruses in the genus Furovirus, Virology, 270, 1, 201-7RJOMREFDiao et al., 1999:10355760RJOHTXDiao et al., 1999, Complete sequence and genome properties of Chinese wheat mosaic virus, a new furovirus from China, J Gen Virol, 80 Pt 5, 1141-5}]. The genome is bipartite, linear, positive sense ssRNA. RNA 1 is about 6–7 kb and RNA 2 about 3.5–3.6 kb. The RNA molecules of SBWMV have a 5′ cap (m7GpppG) and in all of the species where the complete sequences have been determined there is a 3′-terminal tRNA-like structure with a putative anti-codon for valine. The 3′ terminus of SBWMV RNA was shown experimentally to accept valine [{Goodwin and Dreher 1998:9657004RJOHTXGoodwin and Dreher 1998, Transfer RNA mimicry in a new group of positive-strand RNA plant viruses, the furoviruses: differential aminoacylation between the RNA components of one genome, Virology, 246, 1, 170-8}].

Proteins

The capsid comprises (or mostly comprises) multiple copies of a polypeptide of about 19–20.5 kDa. The CPs of SBWMV, Chinese wheat mosaic virus (CWMV), soil-borne cereal mosaic virus (SBCMV) and oat golden stripe virus (OGSV) comprise 176 aa with 76–82% aa identity; they share only 46% identity with that of sorghum chlorotic spot virus (SrCSV). The CP ORF terminates in a leaky (UGA) stop codon that can be suppressed to produce a read-through minor capsid protein (ca. 85 kDa), which is thought to be involved in natural transmission by the plasmodiophorid vector. In SBWMV and CWMV, it has been experimentally shown that a further minor coat protein of 25 kDa is initiated from a CUG codon upstream of the canonical CP AUG but in SBWMV neither minor capsid protein was essential for particle formation or systemic infection [{Shirako 1998:9445077RJOHTXShirako 1998, Non-AUG translation initiation in a plant RNA virus: a forty-amino-acid extension is added to the N terminus of the soil-borne wheat mosaic virus capsid protein, J Virol, 72, 2, 1677-82RJOMREFYamamiya and Shirako 2000:11062037RJOHTXYamamiya and Shirako 2000, Construction of full-length cDNA clones to Soil-borne wheat mosaic virus RNA1 and RNA2, from which infectious RNAs are transcribed In vitro: virion formation and systemic infection without expression of the N-terminal and C-terminal extensions to the capsid protein, Virology, 277, 1, 66-75RJOMREFYang et al., 2016:27357465RJOHTXYang et al., 2016, Functional identification of two minor capsid proteins from Chinese wheat mosaic virus using its infectious full-length cDNA clones, J Gen Virol, 97, 9, 2441-50}].

Genome organization and replication

Genome organization and structure are conserved between members of the species but there are substantial differences in the genomic sequences. SBWMV RNA 1 encodes a 150 kDa protein, a 209 kDa readthrough product and a 37 kDa protein (Figure 2.Furovirus). The 150 kDa protein contains Mtr and NTP-binding Hel motifs. The readthrough protein, in addition, contains RNA polymerase motifs, indicating that these proteins are involved in replication. The 37 kDa protein belongs to the “30K”-like cell-to-cell movement protein superfamily and is thought to be involved in virus movement as it shares some sequence similarity to the MPs of dianthoviruses [{An et al., 2003:14573821RJOHTXAn et al., 2003, Evidence that the 37 kDa protein of Soil-borne wheat mosaic virus is a virus movement protein, J Gen Virol, 84, Pt 11, 3153-63}]. RNA 2 encodes the CP (19 kDa), the sequence of which terminates in a UGA codon that can be suppressed to give a readthrough product of 84 kDa. Also, a 25 kDa polypeptide is initiated from a CUG codon upstream of the CP AUG. A 3′ proximal ORF of RNA 2 encodes a 19 kDa protein that contains seven conserved cysteine residues. This protein is a suppressor of gene silencing [{Te et al., 2005:15740624RJOHTXTe et al., 2005, Soilborne wheat mosaic virus (SBWMV) 19K protein belongs to a class of cysteine rich proteins that suppress RNA silencing, Virol J, 2, 18RJOMREFSun et al., 2013:23458485RJOHTXSun et al., 2013, Identification of the amino acid residues and domains in the cysteine-rich protein of Chinese wheat mosaic virus that are important for RNA silencing suppression and subcellular localization, Mol Plant Pathol, 14, 3, 265-78}]. Products corresponding to the 37 kDa protein and the cysteine-rich 19 kDa protein were not found in in vitro transcription/translation experiments, and these proteins are thought to be expressed from subgenomic mRNAs. Spontaneous deletions in RNA2 occur on successive passage by manual inoculation, and in field isolates in older infected plants, resulting in a shorter CP readthrough product [{Chen et al., 1994:8030253RJOHTXChen et al., 1994, Detection and sequence analysis of a spontaneous deletion mutant of soil-borne wheat mosaic virus RNA2 associated with increased symptom severity, Virology, 202, 2, 921-9RJOMREFChen et al., 1995:7747472RJOHTXChen et al., 1995, An analysis of spontaneous deletion sites in soil-borne wheat mosaic virus RNA2, Virology, 209, 1, 213-7}].

Figure 2.Furovirus. Genome organization of soil-borne wheat mosaic virus (SBWMV). The tRNA structure motifs at the 3′-ends of the RNAs are represented by a dark square, the methyl transferase (Met), Helicase (Hel) and RNA-dependent RNA polymerase (RdRP) motifs by asterisks and the readthrough of the polymerase and coat protein ORFs by RT and an arrow. The major CP (19K) is shown in orange. A minor 25K CP is initiated from an upstream CUG codon. CRP, cysteine-rich protein.

Antigenicity

Virions are immunogenic and members of the different species can be distinguished serologically.

Biology

Furoviruses are found in temperate regions worldwide including the United States of America, Europe, China and Japan. The natural host ranges of furoviruses are narrow and confined to species within the Graminae. SBWMV induces green or yellow mosaic and stunting in winter wheat (Triticum aestivum) causing up to 80% yield loss in severely infected crops. It also may infect barley and rye. SBCMV infects mainly wheat and triticale in Western and Southern Europe and mainly rye in Central and North-Eastern Europe. Both viruses are (not readily) mechanically transmissible to Chenopodium quinoa. OGSV infects oats (Avena sativa) but failed to infect wheat when plants were grown in viruliferous soil. Mechanically OGSV can be transmitted to some Nicotiana and Chenopodium species. SrCSV infects Sorghum bicolor and can be mechanically transmitted to a range of species including Chenopodium quinoa, C. amaranticolor, Nicotiana clevelandii, Arachis hypogaea, Zea mays and T. aestivum.

The furoviruses are soil-borne; Polymyxa graminis has been identified as a vector for SBWMV [{Estes and Brakke 1966:5949390RJOHTXEstes and Brakke 1966, Correlation of Polymyxa graminis with transmission of soil-borne wheat mosaic virus, Virology, 28, 4, 772-4}] and is probably the vector of the other viruses in the genus. Virions are thought to be carried within the motile zoospores. Soil containing the resting spores remains infectious for many years.

Species demarcation criteria

Isolates of different species have less than 75% nt identity for RNA 1 and less than 80% nt identity for RNA 2. SBWMV, SBCMV, CWMV and OGSV can be discriminated also by reactivity with selected monoclonal and polyclonal antibodies. OGSV and SrCSV differ in host range to SBWMV, SBCMV and CWMV. The latter three viruses have similar biological properties and experimental re-assortants of SBWMV (Nebraska), SBWMV (Japan) and SBCMV were infectious [{Miyanishi et al., 2002:12111425RJOHTXMiyanishi et al., 2002, Reassortment between genetically distinct Japanese and US strains of Soil-borne wheat mosaic virus: RNA1 from a Japanese strain and RNA2 from a US strain make a pseudorecombinant virus, Arch Virol, 147, 6, 1141-53}]. With the other viruses this possibility has not yet been checked.